ecological community of the marine intertidal zone (barnacles/balanus glandula/population dynamics/demography)

Vol. 82, pp. 3707-3711, June 1985 Ecology

Larval settlement

rate:

A

leading determinant of structure in an

ecological

community of the marine intertidal zone

(barnacles/Balanusglandula/populationdynamics/demography)

S. GAINES

AND J. ROUGHGARDEN

HopkinsMarineStation, Stanford University, Pacific Grove, CA 93950

Communicatedby L. R. Blinks, January 22, 1985

ABSTRACT Field studies demonstrate that thepopulation structure of the barnacle Balanus glandula differs between locations of high and low larval settlement rate. These

observa-tions,together with results from a model for thedemography of an open, space-limited population, suggest that the settle-ment rate may be a more important determinant of rocky intertidal community structure than is presently realized. Locations with a low larval settlement rate exhibit agenerally low abundanceofbarnacles that varies slightly within years and greatly between years, reflecting yearly differences in settlement. Locations with a high-settlement rate exhibit a generallyhigh abudance ofbarnacles. However, theabundance varies greatly within years with a significantoscillatory com-ponent (period, 30 weeks) and only slightly between years regardless of yearly differences in settlement. At the low-settle-mentlocation mortality of barnacles is independent ofthearea

occupiedby barnacles. At thehigh-settlementlocation mortal-ity is cover-dependent due to increased predation by starfish on areas of high barnacle cover. In both locations the

cover-independent component ofmortality does not vary with age during the first 60 weeks. As assumed in the demographic model, the kinetics of larval settlement can be described as a process in which the rate of settlement to a quadrat is proportional to thefractionof vacant space within thequadrat. Generalizations that the highest species diversity in a rocky

intertidal community is found at locations of intermediate

disturbance, and that competition causes zonation between speciesofthe barnacle genera Balanus andChthamalus,seem toapply only to locations with high-settlement rates.

Many members of ecological communities in the marine intertidal zone have a life history consisting ofpelagically dispersed larvae and sessile, space-limited adults. Familiar examplesinclude barnacles and mussels(1-5).Larvalphases

asshortas2-3 weeksmayleadtotransportof larvae inexcess of 100 km(6-10). Asaresult,recruitment to alocal section of the shoreis from larvae thatlikely originatedatothersites. Hence, alocalsection of shore isanopenpopulationthatis

not satisfactorily treated bythe models ofprimarilyclosed populations applied to terrestrial ecological communities

overthe lastdecade (11-13).

Amodelfor thedemographyandpopulation

dynamics

of

an openpopulation with

space-limited

recruitment has

re-cently beenproposedfor marinepopulationslike barnacles

(14-17). Here we report that qualitative aspects of the

population dynamics of barnacles accord with theoretical expectations of this new model. Specifically, with a low

larval settlement rate, the population tends to approach a

steady-stateabundance. Thatabundance, however, is sensi-tivetostochastic variationinthe settlementrateovertimeor space; we term the condition a "stochastically sensitive"

steady state. With high settlement there is an oscillatory

component to the temporal pattern of abundance that, ac-cording to the model, may be caused in part by the time lag inherent in the space-dependent recruitment of rapidly grow-ingorganisms.

This study also confirms a key assumption of the open-population demographic model, that settlement to vacant

space can be treated as a process in which the rate of

settlement in a quadrat is proportional to the fraction of vacantspaceinit, witha constantof proportionality specific tolocation and time (including season). Further, this study

reveals that disturbance (mortality that removes

space-oc-cupying organisms) is a cover-dependent process for bar-naclessubject to predation by the starfish Pisaster ochraceus andthat thecover-independentcomponentofsurvivorship is

independent ofageforatleast thefirst60weeks of life. Finally, we note that the importance ofthe larval settle-ment rateinpopulationdynamics implies that generalizations about the role ofcompetitionincausingpatternsof zonation through mechanismsrelyingonphysicalcontact (1,2, 18)and the"intermediate disturbance principle,"apostulate that the highest species diversity is found in communities subjectto an intermediate degree of density-independent mortality (19-21), should be qualifiedfor marine intertidal communi-ties. Thesegeneralizations seemtopertain onlytosituations in which the settlementrateis high.

STUDY SITES ANDMETHODS

Thestudy site consistsof rocky intertidal habitat adjacentto

HopkinsMarine StationonMonterey Bay in central Califor-nia. Theabundance of the high intertidal barnacle Balanus glandulavariesfromnearly complete cover onthe seaward marginof the habitattosparse cover onshoreward rocks. We

reportdataprimarilyfromtwosites: KLM,agroupof rocks

nearshore, and Pete's Rock, asimilar group ofrocks, but located betweenKLMand the seawardmargin of the habitat. Thesitesareseparated by""30m.Also, additional datafrom asite, BirdRock,onthe seawardmarginof the habitat and fromasite betweenKLMand Pete's Rockarementioned in theDiscussion.Quadrats (34.6

cm2,

fourpersite)wereplaced in the centerof the Balanus-Endocladia zone(described in ref. 22) and lie atapproximately +1mabovemeanlow low

water. In this zonethe barnacle B. glandula is usually the species occupyingthegreatestamountof space, and thealga Endocladiamuricataalsooccursconspicuously. Inaddition,

the barnacles Chthamalusfissus and Chthamalus dalli and

thealgaGigartina-papillataarealso sessilespaceoccupiers.

Themobileorganismsthat interact with B.glandulaconsist primarily of the starfish P. ochraceus, the Thaidid snails Nucella emarginata, Acanthinapunctulata, and Acanthina

spirata, and the limpets Collisella scabra and Collisella paradigitalis. Atboth Pete's Rock andKLM thefour small quadrats appear to be representative of

"10

m2 of

nearby

substrate with about the same species

composition

and abundance. Theyarethus

descriptive

oftwo

points along

a 3707

Thepublicationcostsof this articleweredefrayedin partbypagecharge

payment.This article must therefore beherebymarked"advertisement" inaccordance with 18U.S.C. §1734 solelytoindicate thisfact.

gradient ofbarnacle abundance and not of two large, discrete regions.

The quadrats were monitored with photographs taken using a camera mounted on a rigid frame. The frame was placed over stainless steel bolts seated in the rock to hold register; the system provides a resolution of 100 am. The outline of the basalareaof allorganisms and the centerof the aperture for all barnacles were digitized from the photo-graphs. The software for digitizing with aHewlett Packard 7221Aplotter-digitizer, and for managing the large data set

involved(>2000individualsinthis study),is writtenin Pascal (Oregon Software Pascal-2) and is available upon request.

Quadrats were monitored daily during August and Sep-tember1982,weekly during April through July 1983 and 1984 (theprincipal settlement season),andbiweekly or monthly at other times. Also, during April to July in 1983 and 1984 photographsonconsecutivelowtides(consecutive low-lows in the mixed semidiurnal schedule that occurs at Hopkins Marine Station) were taken to detectany unusual mortality thatmightaffect barnacles withinhoursafter settlement. The abundance and areaoccupied bybarnacles and other orga-nisms and the growth rate and mortality rate of barnacles

were determined from these data. Mortality caused by

Pisaster predation could be scored by the characteristic discrete patches of basal plates. Thaidid and other predators that leavesingle,empty tests are notdistinguished from each other by these photographic methods.

B. glandula settle ascyprid larvae (aterminal nonfeeding

stage). The cyprids maymove about (23) before taking the location at which they metamorphose into young adults

(spat). They generally metamorphose only on unoccupied space;cyprids metamorphose on thetestsofadult barnacles only ifvacant spaceis <5% (unpublished data). Hence, the settlementrateis expressedasthenumber of cyprids perunit

vacant space perweek.

The relation between settlement rate and free space was determined by subdividing each quadrat into equal sectors and calculating the settlement rate into each sector as a function of the percent free space in it. Tocompare

settle-ment among quadrats that differ markedly in their overall settlementrates, the rateineach sector isexpressed relative

to the settlement in the whole quadrat. If settlement is proportionalto theamount of free space, then thenumber of cyprids settling ina sector(n,) should be

ni

=

sFi,

in which

sis the whole quadrat settlementrate, and

Fi

isthefree space in sector i. Rearranging and including the sector area

(Ai),

ni/(sAi)

=

Fi/Ai.

Therefore, plotting the relative measure of settlement onthe leftas afunction of thepercentfree space inthesector shouldproduce a450line ifsettlementratesare

a simple- linear function of free space. High-settlement quadrats were subdivided into 12 sectors; low-settlement quadrats were subdivided into only 6 sectors.

RESULTS

Uncrowded B. glandula individuals grow in basal area accordingto apower law (basal area = 5.310-5*xl 99, R2 =

0.9873, P << 0.01, units of basal area in cm2 and age in weeks). Thegrowth rates at KLM (where allindividualswere

uncrowded)are identicaltothoseindividuals atPete's Rock

havingonly zero or onecontactingneighbor (F = 1.17,P >

0.25 for comparison of logarithm transformed data). The

individualsat Pete'sRock that contactedtwo or more other

individuals usually showed lower growth rates than

uncrowded individuals.

Weekly survivorship (Ps) was independent ofage (x) at bothsitesfor the firstyear of life (Fig.1).Therewasnohigher

mortality

ofjuvenilesassuggested forthis and other barnacle

species (1,

2,4, 24) despitethepresenceoflimpets. Recruits trackedfromthefirst low tide followingsettlementhad the

1.00r w 0.75 -0-0 50 0. *4

W-*-4I*.-U. i- I-0.00

L

0 15 30 45 60 Age, weeks

FIG. 1. Weekly survivorship versus age for B. glandula. Aster-isks represent data from Pete's Rock, and dots represent data from

KLM. There are no effects of age on survivorship.

same survivorship as older age classes. Barnacle age

ex-plained <5% of the variance in survivorship at each site. For KLM, Px = 0.985 +

(6.71.10-5)x,

R2

= 0.0032, P >0.5;for Pete's Rock,Px =0.939 +

(5.67X10-4)x, R2

= 0.038, P>0.5. Weekly survivorship depends on the amount of free space (Fig. 2). There is a precipitous decline in weekly survivorship when barnacle cover is high caused primarily by predation from the starfish P. ochraceus. In fact, all 21 points repre-senting survivorship values <0.8 in Fig. 2 were associated with discrete patches of basal plates characteristic of Pisaster predation.

Settlement rate at the two sites is directly proportional to the amount of unoccupied space (Fig. 3). More specifically, the relative number of individuals settling in a subsector of a quadrat is directly proportional to the amount of free space in the subsector. Settlement is proportional to free space provided the free space is distributed around existing adults. In contrast, large patches of bare space (>50cm2)tend to be colonized first around the perimeter of the patch (25).

There were large differences in the rate of settlement between sites and between years (Table 1). For each of the 3 years settlement was =20-fold higher at Pete's Rock than at KLM. Also, 1983 had two to four times the recruitment rates of 1982 and 1984 for all quadrats but one (quadrat 4 at KLM).

At KLM there was little within-year variation in free space, yet large between-year changes that mirrored yearly differ-ences in settlement rates (Table 1). A representative trajec-tory is shown in Fig. 4. Notice that the large decline in free

1.00r 0.75 I-0 0. 0e CL 0.501-. 0.25 -0 20 40 60 80 100 %freespace

FIG. 2. Probability of survival through 1 week for B. glandula as afunction ofthepercentage of free space in the quadrat. Data are fromthe Pete's Rock site only. Quadrats at KLM had free space >50% and nodensity-dependent mortality. The high mortality under crowdedconditions primarily represents predation by starfish.

.:. . ."I-1.1. 4Z;, .,w . . .. 7

Proc. Natl. Acad. Sci. USA 82 (1985) 3709

1.00-r

0.75p-v: u CO 100 75 0 0. (A w 50 20 25 0.50 -0.25 -0 20 40 60 80 100 % free space

FIG. 3. Settlement (S) ofB. glandula larvaerelative to the percent free space. Data were obtained by subdividing quadrats and plotting the relative settlement rate against the percent free space in that subquadrat. The approximately450line throughthe origin indicates "mass action" settlement kinetics.

spacecorrespondstothe large1983settlementburst and that the averagefreespacefor1984 is increasingcorrespondingto

the lower settlement of1984. For all KLM quadrats in all years,theyear'saveragefreespace reflectstheintensity of

settlementfor thatyear(Table 1). Anincrease insettlement

relative totheprevious year leads to adecreasein average

free space and vice versa. Indeed, quadrat 4 at KLM, the

quadrat where settlementrates wereaberrantandincreased

Table1. Yearlypatternsof free space availabilityand recruitment

Within-year Recruits, %free space variance asS no. per

Year Mean Variance of totalvariance cm2/week

KLM 1982 88.42 2.46 0.89 0.071 89.01 5.30 1.98 0.063 87.70 15.04 4.41 0.072 94.00 6.33 1.67 0.044 1983 52.89 19.79 7.13 0.28 62.36 23.19 8.68 0.25 61.93 31.01 9.08 0.18 81.77 17.12 4.51 0.059 1984 64.40 19.39 6.98 0.075 65.92 26.54 9.94 0.066 64.04 16.56 4.85 0.053 60.59 22.67 5.97 0.074 Pete's Rock 1982 50.33 207.62 72.94 1.08 43.32 181.61 65.47 1.24 47.82 203.91 84.11 1.38 36.61 188.99 72.69 1.06 1983 50.54 181.33 63.75 4.02 42.89 274.78 99.06 4.36 49.33 220.76 91.07 3.34 42.72 229.23 87.86 3.22 1984 43.54 298.95 105.10 1.51 47.92 153.52 58.84 1.33

Yearsareassumedto startonMay1.Recruitmentis measuredas

the number ofcyprids metamorphosing per cm2 of available free

space per week averaged over the settlement season. Settlement

ratesfor 1982werepartlyestimatedbyextrapolatingbackwards from

barnacle sizedistributionspresent when thestudieswereinitiated.

Datafrom only two quadrats are shownin Pete's Rock for 1984

because theremainingquadratswereinvaded and dominatedbythe

alga E. muricata. Within-year variances can exceed variances

calculated from the entire3-yeartrajectory (asin1984atPete'sRock)

ifvariabilityforaquadratwithin 1 year issubstantially largerthan within theother2 years.

0.60

0.40

0.20

8/82 2/83 8/83 2/84 8/84

FIG. 4. Percent free space (solid line, scale on left vertical axis) and rateof larval settlement (dashed line, scale on right vertical axis) for 2 years in a quadrat from the KLM area at Hopkins Marine Station. 1983 had about four times the settlement of 1984. The trajectory of freespacereflects the settlement history.

progressivelyfrom1982 through 1984, illustrates the

sensitiv-ityof average free space levels to fluctuations in the

magni-tude of settlement. This quadrat showed a progressive

decline inaverage free space each year.

Within-year variances in free space at KLM are consis-tently 1 to 2 orders of magnitude less than total sample

variances for all quadrats (Table 1); most of the total

variability comes from year-to-year differences in average free space. All within-year variances are significantly less

than total variances (varianceratio test onarcsin transformed

data,P <0.001ineach test). Also, at KLM barnacles of all sizes areintermingled withfree space.

AtPete'sRocktheaverage freespace is consistently lower

thanat KLM (t tests; P< 0.01 for each year) and shows no

significant differencebetween years(Table 1) despite similar

3- to 4-fold fluctuations in recruitment as seen at KLM.

Withinyears,however, there are large swings in the amount

offree space. Arepresentative

trajectory

appears in Fig. 5.

Thelarge swingsare notdrivenbybursts ofsettlement,and

there is no correspondence between increasing settlement

and decreasingaverage free space (or vice versa) for any of

the Pete's Rock quadrats (Table 1). Within-year sample

variances for free space are not significantly different (vari-ance ratio test, P > 0.10 for each) from the total sample variance.

Timeseriesanalysis of the freespacetrajectories was used to detect cyclical changes. Autocorrelation functions for

quadrats fromKLMand Pete's RockappearinFig.6. KLM

quadrats show the classicalpattern fornonperiodic random

fluctuations; the autocorrelation rapidly declines tozero as

the lag increases. The autocorrelation for the Pete's Rock quadrats indicate a statistically significant oscillatory com-ponent with a period of ==30 weeks. The cycling process starts with heavy settlement onto vacant space (typically generated byPisasterpredation),followed by rapid growth, andthenbyrecurrenceof starfish predationwhenfreespace

is nearly exhausted. Moreover, free space tends to be distributed in patches thatare later filled by members ofa

single cohort,with the result thatbarnaclesofthesame size tendto occur in patches.

DISCUSSION

Spatial variation in mortality after settlement is not the

primary cause of spatial variation in barnacle density at

Hopkins Marine Station. Density-independent mortality

rates are nearly identical for the two sites. And, when cover-dependent mortalityis alsoconsidered,barnacles have higher overall survivorship at the low-density shoreward sites (Fig. 1). Furthermore, dissections of barnacles during

Ecology:

Roughgarden

I I I 6. 11 1. II 1. f 11 I I

'I

k.- I ,. 10 a 0, 11

C)~~~~~~~~~~~~1

co

5

8/82 2/83 8/83 2/84 8/84

FIG. 5. Percentfreespace(solidline,scaleonleft verticalaxis)

and rate of larval settlement(dashedline,scaleonrightverticalaxis)

for 2years in aquadratfrom the Pete's RockareaofHopkins Marine

Station. The overall settlementrates are -20timesashighasinthe

KLMregion. (Note thechangeinscaleontherightvertical axisfrom

Fig. 4.) Thetrajectory of free space iseffectivelyindependentofthe

settlementhistoryanddisplaysanoscillatory component.

1983 indicated the size-specific reproductiveoutputwasthe same at both sites (unpublished data). The density-independent component ofgrowthisalso thesame atthetwo

sites.Thus, barnaclesperformaswellorbetteratshoreward sites,where their abundance islowest,thanatseawardsites, where theirabundance is higher.

Theprimarydifferenceamong the sites that couldaccount

for theobserved variation in average barnacle abundance is thesettlementrate.Atshorewardsitessettlementislimiting; theabundanceeach yearislow and mirrors the

magnitude

of settlement that year (Table 1). Similar

sensitivity

of a

population's abundancetothesettlementratehasbeennoted in coral reeffish(26, 27), commercial fish stocks(28), and epiphytic bryozoans (29). Atseaward

locations,

settlement rates, though different eachyear,weresufficienttoproduce nearly the same highaverage abundance ofbarnacles each year. Further studies are necessary to determine why the settlementrate varies throughoutthe habitat.

At Pete's Rock, ahigh-settlement location, a significant periodiccomponentin thetemporalpatternofbarnaclecover

was detected (Fig.. 6). According to a model for the demography of an open population with space-limited

re-cruitment(14, 15),a

possible

explanation for the oscillatory component isthe

destabilizing

effect ofgrowth in a sessile

organism

on

population dynamics.

Growth in basal area

effectively introducesatimelag intothepopulation dynamics because recruitment is proportional to the amount of

un-occupied spacecurrentlyavailable andnot tothe amountof space that will beavailablewhen theanimalshave grown to theirexpected area. More larvae thus may settle than the system canultimatelysupport, andcover-dependent mortal-itycanperiodicallyreopen space forsubsequent recruitment. The effect becomes increasingly pronounced as the

settle-ment rateincreases.

Oscillations inbarnacle cover may also be seen in the age distribution. Waves of cohorts are observed (14) as patches offree space undergo the cycle of high recruitment, rapid growth, and finally enhanced mortality when free space is nearly exhausted. Glynn (22), in a study of B. glandula in the early 1960s, presents 3 years of size class distributions (figure 64inref. 22) that clearly show such waves of dominant size classes forasite within a few meters of our present Pete's Rock site. This suggests that the periodicity of barnacle abundancemay have along history at this site.

The large differences in barnacle population dynamics betweenhigh-andlow-settlement sitesposethequestion of whathappensatsites with intermediate settlement rates. We have beenfollowingsixquadratson asomewhat less regular

A -1.00 0°O 1.00KB 0.50 -0.50 -0 10 20 30 40 50

Timelag, weeks

FIG. 6. Autocorrelation functions for percent free space over time.-,Pete'sRock;* * , K,KLM.Quadrats1and2 from eachsite arepresentedinAandquadrats3and4fromeachsitearepresented inB. In Athe quadrats were monitoredfor2 years, and inBthe quadratsweremonitored for75weeks(see Table1legend). Dashed horizontal lines are confidence limits (95%) based on the null hypothesis of white noise fluctuation. Confidence limits inB are slightly largerthaninAduetotheshortertimecourseof thequadrats. The Pete's Rock autocorrelations indicate statistically significant oscillations withaperiod of about 30 weeks. Trends dueto

year-to-year variation in mean free space levels were removed for all quadrats (i.e., the autocorrelation functions are calculated as the products of deviations from yearly means rather than the grand mean). Autocorrelations werecomputedby usingvaluesinterpolated

toachieve weekly intervals during the times whensettlementwas

light and sampling effort reduced. However, confidence intervals for

thenullhypothesiswerecomputedbyusingactualsample sizes.

basis that have had settlement rates between those at KLM and Pete's Rock. Barnacle dynamics have switched with yearlychanges in recruitment rates. In 1982, settlementrates

weregenerally lowand free space was abundant, as at KLM. However,in1983, threeof the quadrats hadsufficientlyhigh recruitment rates that free space levels declined to <30%. Eachof thesethreequadrats attractedpredation by Pisaster, generating the initial phases of the cycling seen at Pete's Rock. Theperiodicity was not sustained, however, because recruitment declinedagain in 1984, andbarnacle abundances have persisted at low levels.

The kinetics of larvalsettlement by barnacle cyprids was found to be a massactionprocess (Fig.3)-thatis, represent-able as an expression of the form: (rate of settlement) = (const) x (free space), in which (const) is a constant of proportionality that reflects many factors, including the abundance oflarvae in the water, the duration of exposure to water, average bulk flow over the surface, and so forth. This

resultis surprising because a large repertoire of behavioral

traits has been shown for larvae that lead to substrate selectivity, gregariousness, spacing, and sensitivity to microclimate (23, 30-32). These capabilities either are not realizedinthefieldfor B.glandula or combining a relatively large number of larvae with individually complex behaviors may maketheaggregatephenomenon describable by a simple

Acad. Sci. USA 82 (1985)

expression.Nonetheless,thefindingsupportstheuseofmass

action formulaein efforts tomodel thedynamics of marine

populations (14, 15).

Mechanisms of mortality that leadtointraspecific density

or coverdependence have been known foryears in marine

systems. "Hummocking," or the bulging ofcrowded

bar-naclesawayfrom the rock surface, canincreaseabarnacle's

susceptibility to removal by waves (4, 33). In this study,

crowded barnacles are more susceptible to predation by starfish than barnacles sparsely intermingled with

unoccu-pied space (Fig. 2). In contrast to the density-independent

mortality causedbywaves orwave-borne logs (4, 34, 35) the

effects of cover-dependent mortality are "biologically

tar-geted"tolocations with highcover.Thus, in this community,

disturbance should not be viewed as an abiotic factorthat

continually resets a community to an earlier point on its

trajectory of development; instead, the disturbance is a

mechanism that depends on the internal state of the

com-munity.

Settlement in the high intertidal community adjacent to

Hopkins Marine Station appearsto play asimportantarole

as postsettlementprocesses suchas predation and

competi-tion. Indeed, the rate of recruitment is a (causally) prior

consideration in determining community structure since its

level selectsthesetof factorsthatsubsequently affect adults. At low settlementthe community is recruitment-limited and sensitiveto stochastic fluctuations in settlement(36, 37). At

high settlement it is a "mosaic of patches" (34, 35) with

intrinsic oscillatory components.

This importance of settlement in determining the

com-munitystructureof rocky intertidal communities implies that

twowell-known generalizations should be qualified as

per-taining onlyto high-settlement communities:

(i) A classical pattern of zonation in the intertidal zone

between barnacles ofthe generaBalanus (Semibalanus) and Chthamalus(1,2,38)is caused by physicalcontact;

individu-alsof Balanuscan overgrow,crush,andprylooseindividuals

ofChthamalus, resulting in Chthamalusremaining only ina zone with physical conditions that Balanus cannot

physio-logically tolerate. For thispattern toform, settlement rates must be consistently high enough to generate extensive

contact among individuals; otherwise the species will have

completelyoverlapping distributions (2). Infact,atHopkins

Marine Station, thecombined abundanceof the barnacles C.

fissus and C. dalli is independent of Balanus abundance

except when free space is nearly exhausted. Specifically,

whenB.glandula occupies <75% ofthesurface,Balanusand Chthamalus densities are uncorrelated (R2 = 0.0049, P> 0.5). Balanus hasasignificant negative effectonChthamalus

abundance where the Balanus abundance is >75% of the

surface. At Hopkins, such high cover of Balanus is only

reachedattheextreme seaward edgeof theintertidalhabitat

(Bird Rock) where settlement rates have generally been

higher than thoseatPete's Rock(unpublished data). Atboth KLM and Pete's Rock, Balanus and Chthamalus have completely overlappingdistributions.

(ii)The"intermediatedisturbanceprinciple,"ahypothesis

that the highest species diversity in acommunity occurs at

some intermediate level ofdisturbance (19, 21), has atacit

assumptionof high settlement(36).Ifsettlementratesarelow

suchthatextensivecontactfailstodevelop among

space-oc-cupiers, then anydecline in diversity caused by apossible

hierarchy in competitive ability cannot be expressed. With low-settlement rates diversity and disturbance may be

in-verselyrelated, regardlessof whetherinterspecific

competi-tion is hierarchical.

We thank Charles Baxter, Lawrence Blinks, Sally Blower,

Stephen Brown, Thomas Hahn, Steven Hamburg, Peggy

Lubchenco, Jane,Lubchenco, Bill Rice, and Rene Toulson for assistance during the course of this research and for comments on the manuscript. We also gratefully acknowledge support from the Department of Energy (Contract EV10108).

1. Connell, J. H. (1961) Ecology 42,710-723.

2. Connell, J. H. (1961) Ecol. Monogr. 31, 61-104. 3. Paine, R. T. (1974) Oecologia 15, 93-120. 4. Dayton, P. K. (1971) Ecol.Monogr. 41, 351-389. 5. Menge, B. A. (1976)Ecol. Monogr. 46, 355-393.

6. Crisp, D. J. (1958) J.Mar. Biol.Assoc. U.K. 37, 483-520. 7. Okubo, A. (1971) Deep-Sea Res. Oceanogr. Abstr. 18,

789-802.

8. Strathmann, R. R. (1974) Am. Nat. 108,29-44.

9. Scheltema, R. S. (1977) in Concepts and Methods of Biostratigraphy, eds. Kauffman, E. G. & Hazel, J. E. (Dowden, Hutchison, and Ross, Stroudsburg, PA), pp. 73-108. 10. Waldichuk, M. (1958) J. Fish. Res. Bd. Can. 15, 1065-1102. 11. May, R. M. (1973)Stability andComplexity in Model

Ecosys-tems (Princeton Univ. Press, Princeton, NJ) 235 pp.

12. Roughgarden, J. (1979) Theory of Population Genetics and Evolutionary Ecology: An Introduction (Macmillan, New York).

13. Diamond, J. &Case, T. (1985) Community Ecology (Harper & Row, New York).

14. Roughgarden, J., Iwasa, Y. & Baxter, C. (1985) Ecology 66, 54-67.

15. Roughgarden, J., Gaines, S. & Iwasa, Y. (1984) in Exploitation ofMarine Communities, ed. May, R. M. (Springer-Verlag,

New York), pp. 111-128.

16. Roughgarden, J. & Iwasa, Y. (1985) Theor. Popul. Biol., in press.

17. Iwasa, Y. & Roughgarden, J. (1985) Theor. Popul. Biol., in press.

18. Wethey, D. (1983)Biol. Bull. 165, 330-341.

19. Paine, R. T. & Vadas, R. L. (1969) Limnol. Oceanogr. 14, 710-719.

20. Connell, J. H. (1975) in EcologyandEvolution of Communi-ties, eds. Cody, M. L. & Diamond, J. M. (Harvard Univ. Press, Cambridge, MA), pp. 460-490.

21. Lubchenco, J. (1978) Am. Nat. 112, 23-39. 22. Glynn, P. (1965)Beaufortia 12, 1-198.

23. Crisp, D. J. (1974) in Chemoreception in Marine Organisms, eds. Grant, P. T. & Mackie, A. M. (Academic, London), pp. 178-265.

24. Hawkins, S. J. (1979) Dissertation (Univ. Liverpool, Liverpool, England).

25. Toulson, R. (1984) Dissertation (Stanford Univ., Stanford,

CA).

26. Victor, B. (1983) Science 219, 419-420.

27. Sale, P. (1984) in Ecological Communities Conceptual Issues andtheEvidence, eds. Strong, D. R., Simberloff, D., Abele,

L. &Thistle, A. B. (Princeton Univ. Press,Princeton, NJ), pp. 478-490.

28. Sissenwine, M. P. (1984) in ExploitationofMarine Communi-ties, ed. May, R. M. (Springer-Verlag, New York)pp. 59-94. 29. Yoshioka, P. M. (1982)Ecology63, 457-468.

30. Strathmann, R. R. & Branscomb, E. S. (1979) inReproductive

Ecology of Marine Invertebrates, ed. Stancyk, S. E. (Univ.

South Carolina, Columbia), pp. 77-89.

31. Lewis, C. A. (1978) in Settlement and Metamorphosis of

MarineInvertebrate Larvae, eds. Chia, F. S. & Rice, M. E.

(Elsevier, New York), pp. 207-218.

32. Wethey, D. (1984) J. Mar. Biol. Assoc. U.K. 64, 687-698. 33. Barnes, H. &Powell, H. (1950) J.Anim. Ecol. 19, 175-179. 34. Levin, S. A. & Paine, R. T. (1974)Proc.Natl.Acad.Sci. USA

71,2744-2747

35. Paine, R. T. & Levin, S. A. (1981) Ecol. Monogr.51, 145-178. 36. Underwood, A. & Denley, E. (1984) inEcological

Communi-ties:Conceptual Issues and the Evidence,eds. Strong, D. R., Simberloff, D., Abele, L. G.&Thistle,A. B.(PrincetonUniv. Press, Princeton, NJ), pp. 151-180.

37. Underwood,A.,Denley,E.&Moran,M. (1983)Oecologia56,

202-219.

38. Wethey, D.S. (1983)Biol. Bull. 165,330-341.