changing recruitment in constant species assemblages: implications for predation theory in...

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Ecology, 78(5), 1997, pp. 1400–1414q 1997 by the Ecological Society of America

CHANGING RECRUITMENT IN CONSTANT SPECIES ASSEMBLAGES:IMPLICATIONS FOR PREDATION THEORY IN INTERTIDAL

COMMUNITIES

CARLOS D. ROBLES

California State University, Los Angeles, California 90032 USA

Abstract. Ecological theory for benthic communities emphasizes intense species inter-actions that depend on the high productivity of sedentary invertebrates. The keystone predatorhypothesis maintains that intense predation by one consumer species is necessary to preventa prolific, competitively dominant prey species from eliminating other species using the sameresource. This study considers the consequences of extreme spatial and temporal variationin the recruitment of a prey species supporting keystone and diffuse predation. Prior exper-iments on rocky shores of Santa Catalina Island, California, USA, demonstrated that predationby spiny lobsters (Panulirus interruptus) maintained a distinctive red algal turf by killingjuvenile mussels (Mytilus californianus and M. galloprovincialis) that otherwise overgrowand replace the algae. In the present study, long-term surveys revealed that high recruitmentof the predominant mussel, M. californianus, occurred only on the most wave-exposed sitesin certain years; mussel recruitment was slight to nil on relatively protected sites in mostyears. A predator exclosure experiment consisting of seven replicates placed along the gradientof wave exposure demonstrated that the effects of predation depended upon the spatial dif-ferences in recruitment rates. Lobsters on wave-exposed sites functioned as keystone pred-ators; on more sheltered sites, little or no predation, whether by lobsters or the fishes andwhelks also foraging on the sheltered sites, was necessary to maintain the algal assemblage.Similar species assemblages can be maintained by markedly different relative levels of crucialecological rates. In the mid-intertidal zone of Santa Catalina Island, the intense speciesinteractions depicted in the keystone predator hypothesis occurred only at productive, highwave exposure locations; low recruitment of mussels elsewhere preempts both predation andthe competition between the mussel and algal assemblages. Thus, red algae dominates rockyshores through different mechanisms over a range of physical conditions. The occurrencesof low mussel recruitment do not appear to be anomalies, but rather a consequence of thelife history of Mytilus californianus.

Key words: algal turfs; California; diffuse predation; growth; keystone predation; Mytilus; Pan-ulirus; productivity; recruitment; spiny lobsters.

INTRODUCTION

From its beginning, experimental ecology empha-sized the effects of intense species interactions drivenby the high reproduction of the participating species.Early experimental tests of ecological theory pittedcompetitors, or predators and their prey, against oneanother in conditions favoring maximum populationgrowth rates. These were laboratory cultures initiallyproviding wall to wall resources and constant physicalconditions (e.g., Gause 1934, Crombie 1946, Huffaker1958, Park 1962). The usual result, extinctions throughintense species interactions, provided empirical supportfor such contemporary theories as the competitive ex-clusion principle (Gause 1934, Hardin 1960) and thetheory of refugia (Gause 1934, Connell 1970, 1975).

The advent of experimental methods to field studieshappened first in rocky intertidal communities, and thetheoretical concerns echoed those of the earlier laboratory

Manuscript received 2 July 1996; revised 11 July 1996; ac-cepted 9 August 1996; final version received 19 September 1996.

experiments. With some exceptions (e.g., Hatton 1938,Frank 1965) most field experiments investigated effectsof intense competition or predation on cool temperateshores with seasonally high production (reviews in Con-nell 1972, Paine 1994, Menge 1995). Much of the theoryfounded upon these experiments addresses mechanismsthat could disrupt the process of competitive exclusion(discussion in Connell 1978, Paine 1994). The ‘‘keystonepredator’’ (Paine 1966, 1974, Menge and Lubchenco1981), ‘‘diffuse predation’’ (Menge and Lubchenco 1981,discussion in Robles and Robb 1993), ‘‘intermediate dis-turbance’’ (Connell 1978, Sousa 1979b, 1984), and ‘‘in-hibition’’ hypotheses (Connell and Slatyer 1977, Sousa1979a) hold one dynamic in common: some agent, wheth-er physical disturbance, a single keystone predator, orperhaps a diverse guild of predators, removes local con-centrations of competitively dominant species, allowingtheir subordinates to grow.

Without removals, high recruitment of sedentaryspecies should precipitate competition for attachmentspace. In the contests among species of algae (Sousa

September 1997 1401CHANGING RECRUITMENT RATES

1979a, Lubchenco 1980, 1986, Schonbeck and Norton1980, Kastendiek 1982), species of barnacles (Connell1961a, b, 1970, Dayton 1971), or mussels, algae, andother invertebrates (Paine 1966, 1974, Paine and Levin1981, Dungan et al. 1982, Underwood et al. 1983, Live-ly and Raimondi 1987, Menge 1992, Robles and Robb1993), dominant competitors recruit in great numbersand either preempt the colonization of less prolific spe-cies or quickly overgrow and displace previously es-tablished, but less robust species. High rates of re-cruitment also figure in the ability of certain dominantspecies to counter predation, because the ‘‘swamping’’(Dayton 1971) of the predators assures that significantnumbers of the juveniles will survive long enough togrow to sizes that resist the subsequent attacks of pred-ators (Connell 1970, Paine 1976, Robles et al. 1990).Thus, substantial productivity, occurring as recruitmentand growth, can drive mechanisms of competition forspace and of size-limited predation, and through thelatter processes certain dominant species acquire andhold space in the rocky shore environment.

The early, formative experiments in rocky shorecommunities supported the view that important featuresof community structure play out in the counterpointbetween competition and predation or disturbance (dis-cussion in Connell 1975, 1978, 1983, Paine 1994).Ironically, continuing experimentation has called intoquestion the feasibility of such generalization (discus-sion in Underwood and Denley 1984, Underwood andFairweather 1988, Foster 1990, Paine 1991, Estes andDuggins 1995). The doubt was fostered, in part, by therealization that the same manipulations repeated at dif-ferent times and places often produce markedly dif-ferent results (e.g., Dayton 1971, Robles and Cubit1981, Keough 1984b, Fairweather and Underwood1991, Paine et al. 1985, Dethier and Duggins 1988,Fairweather and Underwood 1991, Robles and Robb1993, Menge et al. 1994). Reconsideration of experi-mentation with the predators of the mussel Mytilus cal-ifornianus suggests that for this example a resolutionof apparently contradictory results can be found byconsidering the variation in rates of the prey’s recruit-ment.

Paine’s (1966, 1974) original demonstration of key-stone predation in the Mytilus/Pisaster interaction hassince been corroborated by experiments in other inter-tidal communities (Paine et al. 1985) as well as withdifferent species in other ecosystems (discussion inMenge et al. 1994). But, attempts to reproduce the key-stone effect with Pisaster or other predators of M. cal-ifornianus sometimes failed; that is, later removals ofdemonstrated keystone predators produced no signifi-cant increases in mussel abundances (e.g., Robles andRobb 1993, Menge et al. 1994). In the case of the seastars, this has been attributed to scarcity of mussel re-cruitment in unusual years, occurrences that were la-beled anomaly or ‘‘artifact’’ (Paine 1976). Menge etal. (1994) also propose that low recruitment may have

produced some artifact in Pisaster removals at BoilerBay, Oregon, but they argue that natural mussel re-cruitment was appreciable and that the effects of sev-eral consumers were required to limit mussel abun-dances, a case of diffuse predation (Robles and Robb1993). They propose that variation in prey recruitmentaffects the interaction by regulating whether keystoneor diffuse predation occurs at a site.

I repeated removals of spiny lobsters (Panulirusinterruptus) and other mussel predators simulta-neously at the same shore level but different sitesalong a wave exposure gradient at Santa CatalinaIsland, California, USA. The shore level fell alongthe mid-line of a zone of perennial red algae, intowhich juvenile M. californianus recruited to varyingdegrees. I interpret differences among the sites in theoutcome of the removals in light of spatial differ-ences in mussel recruitment at the time of the ex-periment and other, long-term records of mussel re-cruitment. The result shows that whether predatorsare necessary to maintain the cover of algae dependson the recruitment of the mussels. Thus, keystone,diffuse or no predation were required to stop re-placement of algae. Moreover, the extreme variationin productivity of this prey species appears to follownaturally from its life history characteristics; low re-cruitment is neither anomalous nor dependent on ex-treme physical conditions for its occurrence.

Combining the natural variation of recruitment in theaggregate of theory for benthic communities, leads toa consistent interpretation of diverse experimental out-comes, as other authors suggest (e.g., Underwood etal. 1983, Keough 1984b, Underwood and Denley 1984,Gaines and Roughgarden 1985, Menge et al. 1994).

METHODS

Natural history

The mussels Mytilus californianus and M. gallo-provincialis (5 M. edulis, McDonald and Koehn 1988,McDonald et al. 1991) recruited to mid-shore levels ofSanta Catalina and other Channel Islands in greatestnumbers from winter to early spring (Robles 1987; Re-sults: Long-term recruitment surveys). The recruits nes-tled in a turf of coralline and fleshy red algae. If allowedto grow to lengths .1 cm, the juvenile mussels pro-truded from the turf. In most years, this began in spring,at which time they were usually discovered and con-sumed by whelks, Ceratostoma nuttalli and Maxwelliagemma; labrid fishes, Halichoeres semisinctus andSemicossyphus pulcher; and the northern spiny lobster,Panulirus interruptus. In earlier experiments (Roblesand Robb 1993) the dominance of algae appeared tobe maintained by the concerted effects of all consumersin a sheltered area, or by lobsters alone in more wave-exposed areas.

The algal turf consisted of articulated coralline algae(Corallina officianalis var. chilensis) and the delicate

1402 Ecology, Vol. 78, No. 6CARLOS D. ROBLES

FIG. 1. Location of study sites indicated by their numbers.Prevailing northwesterly swells and tidal obstruction currentsfirst hit the shore at the west end of Bird Rock. Depth contoursare given in meters above or below mean lower low water(MLLW).

branching thalli of Gigartina canaliculata, Laurenciapacifica, and other fleshy red algae. The turf formed adense carpet 1–4 cm thick over rock surfaces fromø0.1 to 1.5 m above MLLW (see Murray et al. 1980,Seapy and Littler 1982, Stewart 1982 for a descriptionof species composition and seasonal variation). Thiscover dominated mid-shore levels from sheltered backbays to all but the most wave exposed rocky points,where mussel beds extended down from 12.0 mMLLW, restricting the distribution of the turf to therange from ø0.1 to 0.75 m MLLW.

Study site description

Because community composition and dynamicsmay vary over tidal and wave exposure gradients,the placement the of the sites mattered. One site wasplaced on a horizontal platform in Big FishermanCove, and six sites were placed along a line on ahorizontal platform of a nearby rocky islet, BirdRock (Fig. 1; descriptions in Robles 1987, Roblesand Robb 1993). Sites 1, 2, and 7 had been used forthe ‘‘sheltered,’’ ‘‘moderately exposed,’’ and ‘‘wave-exposed’’ experiments, respectively, in Robles andRobb (1993). The experimental plots fell preciselyalong the horizontal contour of 10.63 m aboveMLLW, dividing the turf zone vertically roughly inhalf. Thus, the comparison among sites maintainedshore-level, topography, and initial species compo-sition, but varied wave exposure. This differs fromother studies with duplicate surveys or experimentsthat confounded shore-level, topographic, and year

differences among sites (e.g., Fairweather and Un-derwood 1991, Robles and Robb 1993, discussion inUnderwood and Petraitis 1993).

Survey methods

Wave exposure.—The study area was protected fromwave action by the mainland to the north and Catalinaitself, which intercepts much of the wave energy orig-inating in summer storms far to the south (Fig. 1).Consequently, the largest input of wave energy cameas westerly swells in fall–winter (United States ArmyCorps of Engineers Report 1986; W. O’Reilly, CoastalData Information Program, personal communication).To provide quantitative estimates of the differences inwave action among the sites, I measured bottom flowspeeds using electromagnetic current meters (Marsh-McBirney 510) and relative total flow over the bottomusing sets of alabaster blocks (Muus 1968).

The current meter records were made as part of aseparate study (C. D. Robles et al., unpublished manu-script). The sensors of the meters stood 30 cm abovethe surface of the turf on metal rods embedded at 10.63m above MLLW, approximately the mid-line of the turfzone. Mean maximum flow speeds were calculatedfrom individual measurements with a time constant of0.2 s taken at 1-s intervals within 2-min periods. The2-min periods began every 15 min from 1 h before to1 h after spring high tides (extreme tides above 1.6 mMLLW). Only two current meters were available, sothat it was not possible to sample all sites simulta-neously. Accordingly, on seven dates from 1989 to1992 the two meters were run simultaneously at a shel-tered location, site 1, and at a relatively more exposedlocation, between sites 4 and 5. Over the same periodof years, asynchronous surveys were made at irregularintervals on sites 1, 2, between sites 4 and 5, and sitesbetween 6 and 7. Unlike the simultaneous sampling ofpaired sites, the latter assessments could have beenbiased by the chance selection of sample dates, becausewave action may vary from day to day.

The total flow of water should be higher on waveexposed sites because flow speeds are higher and great-er wave wash prolongs submergence times. Total flowwas estimated as the percentage loss in mass of ala-baster blocks (Muus 1968). Blocks with dimensions of2 3 4 3 6 cm were bolted to the rock within 20 cmof the border of each of the plots used in the exclosureexperiment. (The blocks were not placed within theplots to keep from damaging the cover of algae.) Theyremained in place for two high tides before they wereremoved and oven dried to constant mass. Two runs ofthe blocks were made: 28 November 1993 and 26March 1994.

Long-term surveys of recruitment.—From 1989 to1995, I estimated recruitment rates at sites 1, 2, and7, the sites of the prior experiments (Robles andRobb 1993). Two 10 m long transects were laid par-allel to the shoreline on each of the sites, and, by


shaving the sandstone substratum with a chisel, allthe attached life was collected in three or four 100-cm2 quadrats spaced randomly along each transect.The samples were examined under a magnifyingglass, the mussels were identified, and their lengthsmeasured in 5-mm increments. I used the density ofmussels ,5 mm long to estimate recruitment. Thesurveys were repeated at quarterly or more frequentintervals from March 1989 through 1992, and theneach March from 1993 to 1995.

The long-term recruitment data were analyzed as atwo-way ANOVA (software by SYSTAT) with site andyear as the factors. Even resorting to elaborate datatransformations (Sokal and Rohlf 1981) the assumptionof equal variances could not be met. Acknowledgingthe violation of the assumption, I present the ANOVAof long-term recruitment with untransformed data be-cause the degrees of bias produced by even extremeheteroscedasticity (Underwood 1981) seem unlikely tochange the decisions to accept or reject, given the verysmall P values that resulted.

A ‘‘divot survey’’ for early postmetamorphic re-cruits.—Analysis of the long-term recruitment surveysraised the question of whether marked spatial differ-ences in mussel recruitment could be attributed to ei-ther (1) differences in postsettlement mortality or (2)differences in larval settlement rate among algal spe-cies, which themselves differed in abundance amongthe sites. On 19 April 1996, three 400-cm2 quadratswere dropped haphazardly within sites 3, 5, and 7.These sites spanned a range of wave exposure and re-cruitment rates. The percent covers of algae were re-corded for each quadrat using the point-intercept meth-od (e.g., Cubit 1984), and then divots of turf, each ø5.0cm2, were chiseled from the rock. Since the divot wassmall, it consisted of only one algal species. Corallinaofficianalis and Gigartina canaliculata were the onlyalgae occurring abundantly on all three sites. Accord-ingly, for each quadrat, five divots were selected atrandom from the covers of (1) Corallina officianalis,(2) Gigartina canaliculata, and (3) one of several otherred algae: Gelidium coulteri, Laurencia pacifica, orRhodoglossum affine, depending on which were mostcommon at a site.

The numbers of mussels 0.2 to 0.7 mm long wererecorded for each divot. This size range included mus-sels that had settled the day of the sample to approx-imately the spring high tide 2 wk earlier (A. Martel,personal communication). Mussel species identifica-tions were made using the criteria of Martel et al.(1993). To determine whether postsettlement mortalitymight have produced the spatial differences in the den-sities of larger recruits, the densities of the early post-metamorphic recruits were compared among the sites.Mean density at a site was estimated by weighting themussel counts from divots of a given algal species bythat alga’s abundances in the quadrats. If postsettlementmortality were solely responsible for the spatial dif-

ferences in densities of larger recruits, then one wouldexpect to find similar densities of early postmetamorph-ic recruits among the sites.

To determine whether early postmetamorphic re-cruitment rates depended on the algal species com-position, a split-plot ANOVA, with quadrats nestedwithin sites, tested the main effects of site and algalspecies on the densities of M. californianus. (Densitiesof M. galloprovincialis were too low to provide tests.)Nesting the quadrats provided an indication of the im-portance of spatial variation within a site.

Experimental methods

Exclosure design.—In January 1993 I marked three20 3 40 cm plots at each of the seven sites. Their exactlocation within a site was haphazard, except for thestipulations that they fall at 0.63 m above MLLW andwithin a 2-m radius, so that their physical conditionsmight be similar. Within each site, a treatment (exclo-sure cage), control for cage effects (open ended cage),and control (open plot) were assigned to the plots bylottery. The cage itself was wire mesh with 1-cm open-ings, stretched over a welded rectangular frame of steelreinforcing bars 1.3 cm (1/2 inch) in diameter, the legsof which were cemented into holes in the rock. Thecontrol for cage effects consisted of the same frameand wire mesh with the end panels removed. Diversobserved lobsters and other predators foraging insidethese ‘‘arch controls.’’

In the prior experiments (Robles and Robb 1993) atthe Cove (site 1) whelks repeatedly penetrated the wiremesh of complete predator removal treatments. Thus,the fact that the effect of treatments was small mighthave been an artifact of the imperfect exclosure, ratherthan low recruitment and growth of prey. In the presentexperiment, I attempted to exclude all whelks by payingcareful attention to the fit of the lower margin of themesh to the irregular stone surface and by placing theexclosures slightly higher (0.63 m as opposed to 0.4 mabove MLLW), a height at which whelk densities werelower (Robles 1987). Despite my efforts, some whelksdid manage to enter exclosures. I examined all 21 plotsat ø1-mo intervals over the course of the experiment.A total of seven Ceratostoma nuttalli were observed inthe 231 records. Six of the seven were small individuals(spire height ,2 cm) that had entered cage exclosures,evidently in response to increased prey densities (seeRobles and Robb 1993 for discussion). Four of the sixwhelks entering exclosures did so at site 1, Big Fish-erman Cove. Whelks were very rare on the turf outsidethe Cove, and the two whelks found in exclosures onBird Rock occurred in the final month of the experiment,long after the differences in mussel density had devel-oped. Therefore, the requirements of the experimentaldesign were met with the exception that whelks mayhave killed some mussels in the predator exclosure atBig Fisherman Cove, site 1.

The changes in percent cover were estimated by the


TABLE 1. Maximum flow speeds (mean 6 1 SE) occurring ,1 h before and after the time ofpredicted extreme high tides in spring and summer, calculated from asynchronous currentmeter records. N 5 number of high tides on which data were logged.

Sites 1 2 3 4 and 5 6 and 7

Speeds (cm/s)NGroup

27.7 6 1.211a

60.0 6 5.12b

61.5 6 5.23b

82.9 6 2.813c

86.5 6 4.913c

Note: Similar means are grouped using Tukey’s hsd test, with the Tukey-Kramer adjustment,and transformed data (Sokal and Rohlf 1981).

FIG. 2. Percentage loss in mass (means and 1 SE) of al-abaster blocks, used to measure total flow over the substra-tum, plotted vs. the alongshore sequence of the sites for sep-arate runs in November 1993 (hatched bars) and March 1994(solid bars).

point intercept method (e.g., Cubit 1984). The esti-mates were made at the beginning of the experiment,February 1993, and its conclusion, February 1994. Ialso made rough visual estimates of percent covers withthe wire mesh in place approximately once every 2 mo.

Initial and final experimental recruitment.—Samplesof the densities of the mussels were also taken fromeach plot immediately before the exclosures were in-stalled and at the conclusion of the experiment. Thesamples were 100-cm2 quadrats scraped up and ex-amined as in the other recruitment surveys. The sam-ples were taken from one corner of the plot, selectedat random, leaving the center of the plot undamagedfor the percent cover surveys. Results of the long-termsurveys of mussel recruitment (see below) indicatedthat peak settlement occurred in winter. The initial sam-pling in the experiment, therefore, served as a measureof the natural recruitment rates of the sites.

The results of the experiment were evaluated withANCOVA. Percent cover or density of Mytilus was thedependent variable, treatment group (open, arch, orcage) was the main effect, and the initial density of

recruits was the covariate. Use of ANCOVA provideda test of the following crucial prediction: if the effectof predator removals depended on prey recruitment,then one would expect to see a significant interactionbetween the main effect and the covariate, the treatment3 recruitment term.

RESULTS

Survey results

Wave exposure.—The estimates of mean maximumflow speeds, measured by current meters on high tidesin spring and summer, confirmed a significant differ-ence in wave exposure between the leeward and wind-ward sites. The synchronous measurements yielded val-ues of 25.5 6 2.4 cm/s and 81.7 6 25.5 cm/s, respec-tively [means 6 1 SE, for the leeward (site 1) andwindward (between sites 4 and 5) locations]. The flowspeeds for the windward location exceeded speeds atthe leeward by at least twofold on all seven sampledates (sign test, N 5 7, P 5 0.0078). Similarly, theasynchronous records indicated a gradient of exposureincreasing from Big Fisherman Cove, to the moderatelyexposed sites in the lee of Bird Rock, to the most ex-posed sites on the west end of Bird Rock (Table 1).

Paralleling the estimates of current speeds, the meanpercentage mass losses of the alabaster blocks in-creased from site 1 to site 7 (Fig. 2, Table 2). However,mean losses in mass for sites 2 and 7 did not matchtheir position in the alongshore sequence of sites (Fig.2). Site 2 was located at the leeward end of the islet.Higher energy waves have longer periods, and therebythey refract around obstacles (Denny 1988). During theNovember 1993 run, I observed large westerly swellsbending around Bird Rock, striking the eastern shorein the area of site 2, which ranked above sites 3 and 4for this run. Mean losses in alabaster mass for site 7ranked below those of site 6. Evidently, a low rockledge just to the windward side of site 7 reduced thewave exposure. Whatever the causes of the variation,the subsequent statistical analyses using wave exposureestimates produced the same inferences regardless ofwhether the alabaster runs were used separately,pooled, or replaced by the alongshore sequence of thesites.

Total flow differed among the sites, but it did notdiffer among the experimental plots within sites (Table2).


TABLE 2. Factorial ANOVA of percentage loss in mass of alabaster blocks measuring totalflow rates. The factors are treatment group (cage, roof, or control), trial (the November 1993and March 1994 runs), and site (the seven locations along shore). R2 5 84%.

Source Sum of squares df Mean square F P

TreatmentTrialSiteThree-way interactionError

8.27636.73

1056.61129.77341.36

216

1216

4.13636.73176.10

10.8121.34

0.1929.85

8.250.51

0.826K0.001K0.001

0.881

Notes: Site 6 had fewer records than the others because two and one blocks were lost, duringthe November 1993 and March 1994 runs, respectively. The limited degrees of freedom pre-vented inclusion of both three-way and two-way interaction terms. However, none of thepossible two-way interactions proved significant in separate models including them but omittingthe three-way interaction.

Long-term recruitment surveys.—The surveys re-vealed consistent differences in mussel recruitmentamong the three sites (Fig. 3). The two relatively shel-tered sites, Big Fisherman Cove (site 1) and the eastend of Bird Rock (site 2), received fewer recruits ofM. californianus and more M. galloprovincialis thandid the wave-exposed west end of Bird Rock, site 7.Since M. californianus was by far the most abundantrecruit, total densities of Mytilus spp. recruits were of-ten .2 orders of magnitude higher on the wave-ex-posed site 7 (Fig. 3).

The alongshore differences were not a consequenceof shore-level differences in recruitment. The shorelevel of the plots was the same for all sites, and surveysof shore-level differences in recruitment (Robles 1987;C. Robles, unpublished data) indicate that the peakrecruitment occurs between 0.50 and 0.75 m aboveMLLW across the wave exposure gradient.

The long-term surveys showed high seasonal andyear to year variation. Peak densities of recruits oc-curred in winter to early spring, but year to year vari-ation appeared to be much greater than seasonal vari-ation (Fig. 3). The temporal variation differed amongsites, so that the sheltered sites apparently had no sig-nificant recruitment of M. californianus for years at atime. The exposed west end of Bird Rock received highbut variable recruitment. These differences are reflect-ed in the significant interaction terms of the ANOVAsrun for the annual, winter samples (Table 3a, b).

The divot survey for early postmetamorphic re-cruits.—The density of early postmetamorphic M. cal-ifornianus increased from 1.20 6 0.46 inds./100 cm2

(mean 6 1 SE) to 39.14 6 9.06 to 200.94 6 33.56inds./100 cm2, respectively, for sites 3, 5, and 7 (ANO-VA of transformed weighted densities: F 5 27.00; df5 2, 6; P 5 0.001). M. galloprovincialis increased from0.34 6 0.34 to 1.60 6 1.60 to 7.78 6 1.88 inds./100cm2, respectively, for sites 3, 5, and 7 (ANOVA ofweighted densities: F 5 7.63; df 5 2, 6; P 5 0.022).These differences, and the observation that newlymetamorphosed mussels (ø300 mm long) were ex-ceedingly rare in the samples from sheltered sites inthis and the other surveys, indicate that the spatial dif-

ferences in recruitment were present from the time ofsettlement.

While very few early recruits were found on anyspecies of algae at the sheltered site 3, they were abun-dant and about twice as common on coralline as onfleshy red algae at the exposed sites (Table 4). Con-sequently, the split-plot ANOVA yielded a significantsite 3 algae interaction term (Table 5b). Corallina of-ficianalis and Gigartina canaliculata showed similarhigh percent covers on all three sites; four other speciesof fleshy red algae were less common (Fig. 4). Thevariation of algal covers within sites was high, so thatonly Rhodoglossum affine was found to differ signifi-cantly among the sites (ANOVA; df 5 2, 6; P 5 0.01).Although some of the among-site difference in meanweighted densities of early postmetamorphic musselscould be attributed differences in percent covers ofalgae alone, the bulk of the difference stems other fac-tors varying along shore. Spatial variation within siteswas not significant (quadrat effect, Table 5a).

Experimental results

Initial experimental recruitment.—At the outset ofthe experiment, Mytilus californianus were the mostabundant recruits in the experimental plots (mean den-sity of M. californianus ,5 mm long 5 26.3 6 11.1inds./100 cm2 [mean 6 1 SE]; N 5 21, i.e., 1 sampleper plot). M. galloprovincialis was comparatively rare(mean density of M. galloprovincialis ,5 mm 5 1.36 0.5 inds./100 cm2, N 5 21), and it occurred in ap-preciable numbers only at the most sheltered site, BigFisherman Cove.

The initial densities of M. californianus recruits, andthus total recruits of Mytilus spp., were positively cor-related with wave exposure (Spearman correlation [rs]between the densities of M. californianus ,5 mm andthe mean percentage mass losses of alabaster blockspooled for both runs for each plot: rs 5 0.68, N 5 21, P5 0.01). Initial recruitment was nil or nearly so for theleeward sites on Bird Rock (sites 2–4) and increased asmuch as two orders of magnitude towards the wave-exposed west end of Bird Rock (sites 5–7, Fig. 5). M.galloprovincialis densities also differed along the shore-


FIG. 3. Densities of recruits of Mytilus californianus (sol-id bar portions) and M. galloprovincialis (hatched portions)at sites 1, 2, and 7 taken at seasonal to annual intervals from1989 to 1995. Data show total Mytilus densities (means and1 SE). (Table 3 ANOVA based on annual, winter samplesonly).

TABLE 3. Factorial ANOVAs of long-term Mytilus recruit-ment surveys. The factors are year (1989, 1995) and site(1, 2, or 7). Records are from one sample each year inwinter, the season that usually showed the greatest musselrecruitment. Data used are inherently heteroscedastic.

SourceSum ofsquares df

Meansquare F P

a) Analysis for M. californianus (R2 5 65%)SiteYearInteractionError

41513.7938439.8568420.2773996.67

26

1294

20756.896406.645701.69

787.20

26.378.147.24

K0.001K0.001K0.001

b) Analysis for M. galloprovincialis (R2 5 42%)SiteYearInteractionError

439.36720.28

1066.523121.63

26

1294

219.68120.05

88.8833.21

6.623.622.68

0.0020.0030.004

line, but only because they were comparatively numerousat site 1, Big Fisherman Cove (Fig. 5, Kruskal–Wallistest, mean densities of M. galloprovincialis: H 5 13.31,df 5 6, P 5 0.038). The six sites on Bird Rock spanneda stretch of shoreline ø175 m long (Fig. 1). Thus, a

marked, regular change in recruitment rates occurred overa remarkably short span of apparently uniform habitat.

Results of exclosure.—At the experiment’s conclu-sion, the densities of M. californianus .1 cm long hadincreased in exclosure plots depending on the level ofinitial recruitment, while densities of the larger musselsin control plots remained nearly nil (Fig. 6). Thus, theprediction that the outcome of predator exclosures de-pends on the initial prey recruitment was verified (sig-nificant treatment 3 recruitment term, Table 6). Re-markably, the linear ANCOVA model accounted fornearly all the variation in densities of M. californianus.1 cm (Table 6, R2 5 99.5%). The treatment 3 re-cruitment interaction was also significant for M. gal-loprovincialis (Fig. 7, Table 7) but because this specieswas comparatively scarce the relationships were not asclear (R2 5 55%).

The survival of masses of Mytilus spp. in the pred-ator exclosures caused changes in percent cover be-cause mussels longer than 1–2 cm overtopped andeventually smothered the woolly algal turf (Fig. 8).The treatment 3 recruitment interaction was signif-icant, and the linear ANCOVA model accounted formuch of the variation in the cover of Mytilus spp.(Table 8, R2 5 90%).

The species composition of the mussel coversmatched the among-site differences in recruitment ofthe two species. M. galloprovincialis covered muchmore of the exclosure plot in Big Fisherman Cove. Themussel cover at the exposed sites consisted almost com-pletely of M. californianus. I observed the covers inexclosures until early spring 1994. At that time, M.californianus covered almost 100% of the plot at site6, and M. galloprovincialis alone covered 25% of theexclosure plot in Big Fisherman Cove.

The changes in percent covers and densities cannotreasonably be attributed to artifacts involving effectsof the wire mesh itself (discussion in Dayton and Oliver1980). The coralline and fleshy algae appear to differin their sensitivity to desiccation and high insolation


TABLE 4. Densities of early postmetamorphic mussels (0.2–0.7 mm long) in the divot survey.Numbers of a mussel species per 5-cm2 divot (means 6 1 SE) are tabulated by site and algalspecies.

Algalspecies† Mussels

Site 3(Leeward)

Site 5(Middle)

Site 7(Windward)

Corallina sp. M. californianusM. galloprovincialis

0.07 6 0.070.07 6 0.07

2.13 6 0.530.40 6 0.24

11.27 6 1.931.33 6 0.47

Gigartina sp. M. californianusM. galloprovincialis

0.13 6 0.090.00 6 0.00

1.07 6 0.320.00 6 0.00

4.94 6 0.570.00 6 0.00

Gelidium sp. M. californianusM. galloprovincialis

0.08 6 0.080.00 6 0.00

0.40 6 0.250.00 6 0.00

······

Pterocladia sp. M. californianusM. galloprovincialis

0.40 6 0.400.00 6 0.00

3.33 6 1.230.00 6 0.00

······

Rhodoglossum sp. M. californianusM. galloprovincialis

······

1.00 6 0.520.00 6 0.00

5.86 6 1.080.14 6 0.14

Laurencia sp. M. californianusM. galloprovincialis

······

······

4.15 6 1.400.17 6 0.17

† At any given site, some of the species of fleshy red algae were too rare to provide enoughsamples for estimates.

TABLE 5. Split plot ANOVA of densities of early post-metamorphic M. californianus in the divot survey.


Meansquare F P

a) Model I ANOVA for the effects of quadrats within sites(R2 5 78%)

SiteAlgae†Site 3 AlgaeQuadrat {Site}

1117.10133.40179.11

14.70

2126

558.55133.40

89.562.45

44.0510.52

7.060.19

·········

0.978Algae 3 Quad-

rat {Site}Error

11.56925.61

673

1.9312.68

0.15 0.988

b) Model II ANOVA for effects of sites and algae (R2 578%)

SiteErrorAlgaeErrorSite 3 AlgaeError

1117.1014.70

133.4011.56

179.1111.56

261626

558.552.45

133.401.93

89.561.93

228.04

69.22

46.47

0.000

0.000

0.000

† Algae included an articulated coralline alga, Corallinaofficianalis, and a fleshy red alga, Gigartina canaliculata;other species of fleshy red algae were omitted because theydid not occur in abundance at every site.

(Seapy and Littler 1982). Yet, a MANCOVA comparingpercent covers of coralline and fleshy algae betweenopen and arch-covered controls at the winter conclu-sion of the experiment was not significant (MANCO-VA: arcsine transformed percentages blocked by site,Hotelling Trace 5 0.899; F 5 2.25; df 5 2, 5; P 50.201). Differences between cage plots and controlsdeveloped in spring and summer, and at a compara-tively low shore level (10.6 m MLLW), conditions inwhich desiccation stress appears to be minimal andpredation pressure the greatest (Robles and Robb1993). The initial recruitment rates of M. californianusin plots selected to receive cages (the January 1993sample) and their final recruitment rates on these plots

(the February 1994 sample) were similar (Pearson r 50.83, P , 0.03), which indicates that the cages did notdirectly affect recruitment.

DISCUSSION

‘‘Recruitment shadows’’ and the intensity ofspecies interactions

Over the last 30 yr, benthic ecologists emphasizedintense interactions among sedentary species in thepostrecruitment phase of their life cycles (reviews inConnell 1972, 1975, Menge and Sutherland 1976, Un-derwood and Denley 1984, Paine 1994, Menge 1995).The keystone predator paradigm, intermediate distur-bance hypothesis, and some other theories arising inthis period provided explanations for the coexistenceof the many species competing for the same, potentiallylimiting resource. The impetus for these theories maybe traced back to the dilemmas presented by the com-petitive exclusion principle (Gause 1934, Hardin1960), and thence back to the speculations of Darwin(1859) and Malthus (1798) about the consequences ofgeometric increase of populations. Laboratory cultures,the first tests of the emerging corpus of ecological the-ory, confirmed the effects of intense species interactionduring rapid population growth (e.g., Gause 1934,Crombie 1946, Huffaker 1958, Park 1962). Thus, thepotential for high reproduction of species has servedhistorically as a foil for theoretical discourse, and, nec-essarily, directed attention to intense species interac-tions. Whether this potential is manifest in a givennatural population is a pivotal ecological question.

For benthic species with planktotrophic larvae, in-teractions on the shore ensue only after a sequence ofcrucial events in their early life history. The sequenceruns from the spawning of adults, to planktonic de-velopment, to the recruitment of the larvae to shorepopulations, to the grow-out of these young to suffi-


FIG. 4. Mean percent covers of algal species at study sitesin the divot survey.

FIG. 5. Mussel recruitment (inds./100 cm2 plot) at theoutset of the experiment [means and 1 SE]. Heights of barsrepresent mean total mussels; shadings represent relative pro-portions of the two species: M. californianus (solid) and M.galloprovincialis (hatch). The bars are arranged on the x-axisby rank of mean total flow (fall and winter means averagedfor each site).

FIG. 6. Densities of M. californianus .1 cm at the con-clusion of the experiment plotted on log scales as a functionof the species’ initial recruitment. Circles 5 open plots, tri-angles 5 arch covered plots, and squares 5 cage coveredplots. Site numbers appear inside symbols. Overlapping sym-bols have been offset to make site numbers legible.

cient sizes to exert competitive effects. Production maybe diminished at any link in the chain preceding re-cruitment. Adults may find themselves without nearbymates (Pennington 1985) or sufficient resources to re-produce. Zygotes and larvae may be advected away(Parrish et al. 1981, Roughgarden et al. 1988, Bailey1991, Gaines and Bertness 1992, Hobbs et al. 1992),may starve or die by planktonic predators (Gaines etal. 1985) before reaching the habitats of the adults, andthose larvae finally reaching the shore may grow poor-ly, depending on the resources provided by the habitat.Except for predation in the plankton, none of the mech-anisms necessarily involve intense species interactions.Yet, working separately or together, these mechanismsappear responsible for the pronounced variation in re-cruitment rates documented for benthic invertebrates(Caffey 1985, Hughes 1990, Raimondi 1990, Bertness

et al. 1992; see Gaines and Bertness 1992, Connell1985 for reviews). Therefore, whether intense postre-cruitment competition or predation occurs on the shoremay ultimately depend on antecedent factors affectingrates of recruitment.


TABLE 6. ANCOVA for densities of M. californianus .1cm long at the conclusion of the recruitment variation ex-periment. The main effect is treatment group (cage, roof,open control); the covariate is the initial experimental re-cruitment of this species. R2 5 99.5%.


Meansquare F P

TreatmentRecruitmentInteractionError

1.119085.43

13587.05108.63

212

15

0.569085.436793.53

7.24

0.081254.59

938.11

······

0.001

Notes: Spearman correlations (rS) between initial recruit-ment and densities of M. californianus .1 cm are rS 5 0.54,0.61, and 0.94*, respectively, for open, arch, and cage treat-ments.

* Significant under procedurewise a 5 0.05, employing theBonferroni correction.

TABLE 7. ANCOVA for densities of M. galloprovincialis .1cm long (analysis as in Table 6). R2 5 55%.


Meansquare F P

TreatmentRecruitmentInteractionError

0.599.71

19.6135.71

212

15

0.309.719.812.38

0.1244.084.12

······

0.038

FIG. 8. Triangular coordinate diagrams of the relativecover of Mytilus spp., fleshy red algae, and the coralline algaCorallina officianalis at the end of the experiment (February1994). The three species groups accounted for $80% of thetotal cover of each plot. Symbols near the center of each largetriangle represent approximately equal coverages of the threetypes of cover; symbols near the apex represent a nearly con-tinuous cover of the Mytilus spp. assemblage. Circles 5 openplots, triangles 5 arch covered plots, and squares 5 cagecovered plots. The top figure pertains to open plots (control),the middle to arch covered plots (control), and bottom to cagecovered plots (treatment).

FIG. 7. Densities of M. galloprovincialis .1 cm at theconclusion of the experiment plotted on log scales as a func-tion of this species’ initial recruitment. Circles 5 open plots,triangles 5 arch covered plots, and squares 5 cage coveredplots. Site numbers appear inside symbols. Overlapping sym-bols have been offset to make site numbers legible, as in thecluster at the origin.

Recognizing the potential limitations of theory basedsolely on postrecruitment interactions, benthic ecolo-gists recently focused their attention on the effects ofrecruitment variation on the structure of benthic pop-ulations (e.g., Keough 1984a, b, Caffey 1985, Gaineset al. 1985, Gaines and Roughgarden 1985, Sutherlandand Ortega 1986, Sutherland 1987, 1990, Davis 1988,Hughes 1990, Raimondi 1990, Bertness et al. 1992,Menge 1992, Robles et al. 1995). Both theory and em-pirical evidence argue that variation in recruitment canregulate the intensity of postrecruitment interactions.

The results from Santa Catalina Island suggest thatconstraints are sometimes imposed early enough in thesequence of events leading to recruitment to preclude


TABLE 8. ANCOVA for percent covers of Mytilus spp. inthe experiment. Sum of squares was calculated for 103 3the arcsine transform (Sokal and Rohlf 1981). The maineffect is treatment group, and the covariate is initial re-cruitment of Mytilus spp. R2 5 90%.


Meansquare F P

Treatment 512.87 2 256.43 2.13 ···Recruitment 5303.07 1 5303.07 43.98 ···Interaction 8432.52 2 4216.26 34.97 K0.0001Error 1808.60 15 120.57

Note: Spearman correlations between initial recruitmentand the transformed percent covers are rS 5 0.72, 0.16, and0.92*, respectively, for open, arch, and cage treatments.

* Significant under procedurewise a 5 0.05, employing theBonferroni correction.

intense species interactions. The analysis of the den-sities of early postmetamorphic recruits suggests thatthe spatial differences in initial experimental recruit-ment probably resulted directly from differences in set-tlement rate, rather than postsettlement mortality. I didnot directly observe settlement, and the proximal mech-anisms causing the spatial differences in early post-metamorphic recruitment remain a matter of specula-tion. Once established, juvenile mussels either suc-cumb to predation or exert competition.

A finding that species have no impact in habitats inwhich they do not occur would have been trivial. Anoteworthy feature of the present work is that extremevariation in the rates of recruitment of the dominantprey occurred over a small distance within a specifichabitat, in which the composition of the characteristicspecies assemblage remained relatively constant fromyear to year across a range of physical conditions.

Observations of marked alongshore differences inrates of recruitment of a species are common (e.g.,Underwood et al. 1983, Caffey 1985, Gaines et al.1985, Kendall et al. 1985, Sutherland and Ortega 1986,Raimondi 1990, Sutherland 1990, Bertness et al. 1992).Areas of chronically low recruitment next to consis-tently high recruitment areas within the same habitat Iterm ‘‘recruitment shadows.’’ The existence of recruit-ment shadows suggests that significant and predictabledifferences in the intensity of postrecruitment inter-actions can occur.

Petraitis (1974, 1978) also found a positive corre-lation between wave exposure and the relative abun-dances of M. californianus recruits. He found a neg-ative correlation for M. galloprovincialis (5M. edulis).He questions Harger’s (1972) hypothesis that M. gal-loprovincialis competitively excludes M. californianusin sheltered locations, noting that recruitment patternsshould preclude the interaction over much of the waveexposure gradient. Analogously, predation on musselsor competition between mussels and algae should benegligible in the recruitment shadow at Bird Rock. Butat site 1, unlike Petraitis’ (1974, 1978) comparison, I

found that the recruits of different Mytilus speciessometimes commingled (Fig. 3; see also Menge et al.1994, Robles et al. 1995).

The positive relationship between wave exposureand high recruitment may hold some advantage for M.californianus. If recruits grow slowly in sheltered ar-eas, then individual M. californianus should (1) in-crease size and hence reproductive output relativelyslowly and (2) remain vulnerable to predators for pro-longed periods. Recruiting to sites with high wave ex-posure should increase the likelihood that predatorswamping (Dayton 1971) will be successful, becausefast growing mussels remain vulnerable for a compar-atively short period, and hydrodynamic stresses caninterrupt predator foraging more frequently (Menge1978a, b, Robles and Robb 1993; C. D. Robles et al.,unpublished manuscript). This explanation depends onthe positive relationship between wave exposure andmussel growth rates (Leigh et al. 1987, Robles andRobb 1993, Sherwood-Stephens 1993) and on size lim-its to predation for M. californianus (Harger 1970,1972, Dayton 1971, Paine 1974, Robles et al. 1990).Size-limited predation characterizes the interaction ofM. californianus with all of its predators, and the ex-planation may apply throughout its range, beyond thenorthern distribution limit of the lobsters at Point Con-ception, California.

Judging by the distribution of adults (see, for ex-ample, Stephenson and Stephenson 1972), M. califor-nianus is successful only on rocky shores with highwave exposure. On sites 6 and 7, beds of adult M.californianus do occur at higher shore levels, and onthe same shore level 5–10 m to the windward. At hightide, I have observed lobsters roaming freely from theexperimental (turf) sites to the extreme vertical andhorizontal limits of the mussel beds. In the absence ofabsolute spatial or age/size refugia (Robles et al. 1990),the dynamics of prey production and consumption ev-idently tip in favor of the mussels at the wave-beatenextreme of the exposure gradient. Thus it appears thatthe tendency of M. californianus to recruit most heavilyto wave-exposed sites is an advantageous feature of alife history characterized by size-limited predation andindeterminate growth rates (Sebens 1987) that dependon wave exposure.

Changing rates, constant assemblages, andecological generalities

Depending on one’s perspective, field experimentsare blessed or damned by variation. The same manip-ulations often produce different results, and in somecases the differences are extreme (discussion in Dayton1971, Paine 1976, Underwood and Petraitis 1993; otherexamples in Robles and Cubit 1981, Keough 1984b,Dethier and Duggins 1988, Fairweather and Under-wood 1991, Robles and Robb 1993, Menge et al. 1994).Arising unexpectedly yet repeatedly, such variation hasled to debate over whether generalization from field


studies is possible or even desirable at present (see forexample Underwood and Denley 1984, Foster 1990,Paine 1991, Estes and Duggins 1995).

Fairweather and Underwood (1991) describe varia-tion similar to the Catalina findings: the effect of pred-ator removals varied among replicates at different lo-cations. In their case, the predators were whelks (Mor-ula marginalba) preying on barnacles, tube worms, andother sedentary invertebrates on rocky shores of south-eastern Australia. They attribute the variation to pre-sumed small scale differences in wave stress, micro-climate, topography, and historical factors that mightinfluence the intensity of predation.

The composition of the predator fauna can alsochange from site to site within an intertidal habitat (e.g.,Robles and Robb 1993 and Menge et al. 1994). In priorexperiments at site 7, exclosure of lobsters with largemesh (2.5-cm2 opening) cages, produced marked in-creases in mussels, whereas whelks (Ceratostoma nut-talli and Maxwellia gemma) passed through the meshand prevented similar results in large mesh exclosureexperiments at site 1 (Robles and Robb 1993). Whetherthe core predators are lobsters (Robles and Robb 1993)or sea stars (Menge et al. 1994), predation can shiftfrom ‘‘keystone’’ to ‘‘diffuse’’ over short distancesfrom the wave exposed to sheltered portions of thehabitat.

The variation among replicates in the present ex-periment cannot be attributed to either spatial variationin physical stresses affecting the predators, or to shift-ing composition of the predator fauna. The lobsterswere present only at high tide, and wave action mighthave hindered their foraging at exposed sites (C. D.Robles et al., unpublished manuscript). However, what-ever stresses where present did not prevent them fromeliminating the mussels even at the comparatively waveexposed sites 5–7. The variation among the replicatesoccurred within the exclosures, and therefore could nothave been caused by differences in the intensity ormechanisms of predation, although such differencesmay arise along with the shift from diffuse to keystonepredation along the wave exposure gradient. Rather,differences in the recruitment of mussels accounted formost of the variation among replicates.

M. galloprovincialis did recruit to site 1, and thisspecies replaced some of the turf in the predator ex-closure (see also Robles and Robb 1993). However,this cover was lost immediately upon re-exposure topredators (C. D. Robles, personal observation; Roblesand Robb 1993). M. galloprovincialis and closely re-lated congeners (M. trossulus and M. edulis) possess athin shell, and they remain vulnerable to, and preferredby, mussel predators throughout their lives (Harger1970, 1972, Elner 1978, Seed 1979). Thus, low inten-sity diffuse predation, i.e., low densities of lobsters,fishes, and whelks together, could be expected to pre-vent the establishment of a perennial cover of musselsof this species. In contrast, a prior lobster removal ex-

periment at site 7 (Robles and Robb 1993) produced adense cover of predominantly large (.5 cm) M. cali-fornianus that persisted indefinitely after re-exposureto predators.

I have done four predator removal trials on site 1 infour different years from 1982 to 1994. Whelks pen-etrated exclosures, and they probably affected the ratesat which the mussel replaced the turf. But, consideringthe outcome of the surveys and the outcome of exclo-sures where no whelks were present, it seems reason-able to attribute the failure of the removals in verysheltered areas to produce a persistent cover of musselsto the low recruitment of M. californianus.

Two prior studies provide consistent interpretationsof spatial differences in the effect a keystone predatorby considering variation in prey recruitment. Menge etal. (1994) propose that the occurrence of keystone pre-dation by sea stars (Pisaster ochraceus) on mussels(Mytilus spp.) is associated with high ‘‘food inputrates,’’ i.e., the recruitment of all sedentary prey spe-cies including mussels and barnacles; low food inputfavors diffuse predation. Presumably, greater preyavailability promotes greater biomass of the keystonepredator’s population by elevating its settlement,growth rates, or densities via alongshore movements(see Robles et al. 1995 for discussion). In the secondstudy, working with observational evidence alone, Es-tes and Duggins (1995) propose that the rates at whichkelp beds recover following reintroduction of sea otters(Enhydra lutris) depends, in part, on the recruitmentrates of herbivorous sea urchins (Strongylocentrotusspp.). In regions where urchin recruitment is high, theotters, which prefer to consume larger urchins, reducegrazing pressure comparatively slowly, and the recov-ery of the kelp beds is retarded relative to regions withlower urchin recruitment rates.

Variation in recruitment rates affects experimentalassessments of the effects of postrecruitment factors,and the generalities these assessments support (see alsoUnderwood and Petraitis 1993, Menge et al. 1994).Depending on the levels of mussel recruitment, key-stone predation, diffuse predation, or no predation maybe required to maintain the distinctive assemblage ofalgae at different times and locations along the shore-line of Santa Catalina Island.

ACKNOWLEDGMENTS

Suggestions by S. Gaines, R. Nakamura, and an anonymousreviewer greatly improved drafts of the manuscript. M. Al-varado, C. Chauteco, C. Hernandez, M. Maiten, N. Nipata-rudi, K. Pan, R. Sherwood-Stephens, and F. Villeda helpedwith the field work. The expense of the project was borne bythe National Science Foundation, nos. RII8804679 andOCE9217235001. This is contribution no. 175 of the Publi-cations of the Catalina Marine Science Center.

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